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Title: Selective molecular transport through the protein shell of a bacterial microcompartment organelle

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [3];  [3];  [1];  [4];  [1]
  1. Iowa State Univ., Ames, IA (United States). Roy J. Carver Dept. of Biochemistry, Biophysics, and Molecular Biology
  2. Univ. of California, Los Angeles, CA (United States). Molecular Biology Inst.
  3. Univ. of California, Los Angeles, CA (United States). UCLA-DOE Inst. for Genomics and Proteomics
  4. Univ. of California, Los Angeles, CA (United States). Molecular Biology Inst. UCLA-DOE Inst. for Genomics and Proteomics. Dept. of Chemistry and Biochemistry
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Bacterial microcompartments are widespread prokaryotic organelles that have important and diverse roles ranging from carbon fixation to enteric pathogenesis. Current models for microcompartment function propose that their outer protein shell is selectively permeable to small molecules, but whether a protein shell can mediate selective permeability and how this occurs are unresolved questions. In this paper, biochemical and physiological studies of structure-guided mutants are used to show that the hexameric PduA shell protein of the 1,2-propanediol utilization (Pdu) microcompartment forms a selectively permeable pore tailored for the influx of 1,2-propanediol (the substrate of the Pdu microcompartment) while restricting the efflux of propionaldehyde, a toxic intermediate of 1,2-propanediol catabolism. Crystal structures of various PduA mutants provide a foundation for interpreting the observed biochemical and phenotypic data in terms of molecular diffusion across the shell. Finally and overall, these studies provide a basis for understanding a class of selectively permeable channels formed by nonmembrane proteins.

Research Organization:
Iowa State Univ., Ames, IA (United States); Univ. of California, Los Angeles, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health (NIH) (United States)
Grant/Contract Number:
AC02-06CH11357; 5P41RR015301-10; 8 P41 GM103403-10; R01AI081146; T32-GM008496
OSTI ID:
1172992
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 10; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
ENGLISH
Citation Metrics:
Cited by: 84 works
Citation information provided by
Web of Science

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Cited By (29)

Coenzyme B12 synthesis as a baseline to study metabolite contribution of animal microbiota journal June 2017
Bacterial microcompartments: catalysis-enhancing metabolic modules for next generation metabolic and biomedical engineering journal October 2019
Functional protein shells fabricated from the self-assembling protein sheets of prokaryotic organelles journal January 2020
Engineering formation of multiple recombinant Eut protein nanocompartments in E. coli journal April 2016
Bacterial Microcompartments journal January 2007
Development of an efficient technique for gene deletion and allelic exchange in Geobacillus spp. journal April 2017
Encapsulation mechanisms and structural studies of GRM2 bacterial microcompartment particles journal January 2020
Encapsulation of multiple cargo proteins within recombinant Eut nanocompartments journal July 2016
Bio-engineering of bacterial microcompartments: a mini review journal June 2019
The function of the PduJ microcompartment shell protein is determined by the genomic position of its encoding gene: Function of the PduJ microcompartment shell protein journal June 2016
Effect of bio-engineering on size, shape, composition and rigidity of bacterial microcompartments journal November 2016
A Bacterial Microcompartment Is Used for Choline Fermentation by Escherichia coli 536 journal March 2018
All-atom normal mode dynamics of HIV-1 capsid journal September 2018
Engineering bacterial microcompartments with heterologous enzyme cargos journal September 2016
Fast normal mode computations of capsid dynamics inspired by resonance journal April 2018
Localization of Proteins to the 1,2-Propanediol Utilization Microcompartment by Non-native Signal Sequences Is Mediated by a Common Hydrophobic Motif journal August 2015
Engineering the PduT shell protein to modify the permeability of the 1,2-propanediol microcompartment of Salmonella journal December 2019
Enzymatic reactions in confined environments journal May 2016
Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways: Bacterial microcompartments journal August 2015
Transfer and analysis of Salmonella pdu genes in a range of Gram-negative bacteria demonstrate exogenous microcompartment expression across a variety of species journal October 2017
HIV-1 uses dynamic capsid pores to import nucleotides and fuel encapsidated DNA synthesis journal August 2016
Control of enzyme reactions by a reconfigurable DNA nanovault journal October 2017
The Phenix software for automated determination of macromolecular structures journal September 2011
Proteomic Delineation of the ArcA Regulon in Salmonella Typhimurium During Anaerobiosis journal July 2018
Bacterial microcompartments journal March 2018
Engineered synthetic scaffolds for organizing proteins within the bacterial cytoplasm journal December 2017
The N Terminus of the PduB Protein Binds the Protein Shell of the Pdu Microcompartment to Its Enzymatic Core journal January 2017
Bacterial Microcompartments journal October 2010
Apparent size and morphology of bacterial microcompartments varies with technique journal March 2020

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
microcompartment
protein channel
carboxysome
Salmonella
B12